Abstract

Introduction

Many mammals have evolved highly adapted hearing associated with ecological specialisation.
Of these, bats possess the widest frequency range of vocalisations and associated
hearing sensitivities, with frequencies of above 200 kHz in some lineages that use
laryngeal echolocation. High frequency hearing in bats appears to have evolved via
structural modifications of the inner ear, however, studying these minute features
presents considerable challenges and hitherto few such attempts have been made. To
understand these adaptations more fully, as well as gain insights into the evolutionary
origins of ultrasonic hearing and echolocation in bats, we undertook micro-computed
tomography (μCT) scans of the cochleae of representative bat species from 16 families,
encompassing their broad range of ecological diversity. To characterise cochlear gross
morphology, we measured the relative basilar membrane length and number of turns,
and compared these values between echolocating and non-echolocating bats, as well
as other mammals.

Results

We found that hearing and echolocation call frequencies in bats correlated with both
measures of cochlear morphology. In particular, relative basilar membrane length was
typically longer in echolocating species, and also correlated positively with the
number of cochlear turns. Ancestral reconstructions of these parameters suggested
that the common ancestor of all extant bats was probably capable of ultrasonic hearing;
however, we also found evidence of a significant decrease in the rate of morphological
evolution of the basilar membrane in multiple ancestral branches within the Yangochiroptera
suborder. Within the echolocating Yinpterochiroptera, there was some evidence of an
increase in the rate of basilar membrane evolution in some tips of the tree, possibly
associated with reported shifts in call frequency associated with recent speciation
events.

Conclusions

The two main groups of echolocating bat were found to display highly variable inner
ear morphologies. Ancestral reconstructions and rate shift analyses of ear morphology
point to a complex evolutionary history, with the former supporting ultrasonic hearing
in the common bat ancestor but the latter suggesting that morphological changes associated
with echolocation might have occurred later. These findings are consistent with theories
that sophisticated laryngeal echolocation, as seen in modern lineages, evolved following
the divergence of the two main suborders.